DOI QR코드

DOI QR Code

Breastfeeding and Ovarian Cancer Risk: a Systematic Review and Meta-analysis of 40 Epidemiological Studies

  • Li, Da-Peng ;
  • Du, Chen ;
  • Zhang, Zuo-Ming ;
  • Li, Guang-Xiao ;
  • Yu, Zhi-Fu ;
  • Wang, Xin ;
  • Li, Peng-Fei ;
  • Cheng, Cheng ;
  • Liu, Yu-Peng ;
  • Zhao, Ya-Shuang
  • Published : 2014.06.30

Abstract

The present systematic review and meta-analysis was conducted to assess any association between breastfeeding and the risk of ovarian cancer. A systematic search of published studies was performed in PUBMED and EMBASE and by reviewing reference lists from retrieved articles through March 2013. Data extraction was conducted independently by two authors. Pooled relative risk ratios were calculated using random-effect models. Totals of 5 cohort studies and 35 case-control studies including 17,139 women with ovarian cancer showed a 30% reduced risk of ovarian cancer when comparing the women who had breastfed with those who had never breastfed (pooled RR = 0.70, 95% CI: 0.64-0.76; p = 0.00), with significant heterogeneity in the studies (p = 0.00; I2 = 76.29%). A significant decreasd in risk of epithelial ovarian cancer was also observed (pooled RR = 0.68, 95% CI: 0.61-0.76). When the participants were restricted to only parous women, there was a slightly attenuated but still significant risk reduction of ovarian cancer (pooled RR = 0.76, 95% CI: 0.69-0.83). For total breastfeeding duration, the pooled RRs in the < 6 months, 6-12 months and > 12 months of breastfeeding subgroups were 0.85 (95% CI: 0.77-0.93), 0.73 (95% CI: 0.65-0.82) and 0.64 (95%CI: 0.56-0.73), respectively. Meta-regression of total breastfeeding duration indicated an increasing linear trend of risk reduction of ovarian cancer with the increasing total breastfeeding duration (p = 0.00). Breastfeeding was inversely associated with the risk of ovarian cancer, especially long-term breastfeeding duration that demonstrated a stronger protective effect.

Keywords

Breastfeeding;ovarian cancer;risk reduction;meta-analysis

References

  1. Zhang M, Xie X, Lee AH, Binns CW (2004). Prolonged lactation reduces ovarian cancer risk in Chinese women. Eur J Cancer Prev, 13, 499-502. https://doi.org/10.1097/00008469-200412000-00006
  2. Wilailak S, Vipupinyo C, Suraseranivong V, et al (2012). Depot medroxyprogesterone acetate and epithelial ovarian cancer: a multicentre case-control study. BJOG, 119, 672-7. https://doi.org/10.1111/j.1471-0528.2012.03298.x
  3. Yen ML, Yen BL, Bai CH, Lin RS (2003). Risk factors for ovarian cancer in Taiwan: a case-control study in a low-incidence population. Gynecol Oncol, 89, 318-24. https://doi.org/10.1016/S0090-8258(03)00088-X
  4. Zhang M, Lee AH, Binns CW (2004). Reproductive and dietary risk factors for epithelial ovarian cancer in China. Gynecol Oncol, 92, 320-6. https://doi.org/10.1016/j.ygyno.2003.10.025
  5. Titus-Ernstoff L, Rees JR, Terry KL, Cramer DW (2010). Breastfeeding the last born child and risk of ovarian cancer. Cancer Causes Control, 21, 201-7. https://doi.org/10.1007/s10552-009-9450-8
  6. Stroup DF, Berlin JA, Morton SC, et al (2000). Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA, 283, 2008-12. https://doi.org/10.1001/jama.283.15.2008
  7. Su D, Pasalich M, Lee AH, Binns CW (2013). Ovarian cancer risk is reduced by prolonged lactation: a case-control study in southern China. Am J Clin Nutr, 97, 354-9. https://doi.org/10.3945/ajcn.112.044719
  8. Titus-Ernstoff L, Perez K, Cramer DW, et al (2001). Menstrual and reproductive factors in relation to ovarian cancer risk. Br J Cancer, 84, 714-21. https://doi.org/10.1054/bjoc.2000.1596
  9. Tsilidis KK, Allen NE, Key TJ, et al (2011). Oral contraceptive use and reproductive factors and risk of ovarian cancer in the European Prospective Investigation into Cancer and Nutrition. Br J Cancer, 105, 1436-42. https://doi.org/10.1038/bjc.2011.371
  10. Tung KH, Goodman MT, Wu AH, et al (2003). Reproductive factors and epithelial ovarian cancer risk by histologic type: a multiethnic case-control study. Am J Epidemiol, 158, 629-38. https://doi.org/10.1093/aje/kwg177
  11. Wang KL, Liu CL, Zhuang Y, Qu HY (2013). Breastfeeding and the risk of childhood Hodgkin lymphoma: a systematic review and meta-analysis. Asian Pac J Cancer Prev, 14, 4733-7. https://doi.org/10.7314/APJCP.2013.14.8.4733
  12. Weiderpass E, Sandin S, Inoue M, et al (2012). Risk factors for epithelial ovarian cancer in Japan - results from the Japan Public Health Center-based Prospective Study cohort. Int J Oncol, 40, 21-30.
  13. Whittemore AS, Harris R, Itnyre J (1992). Characteristics relating to ovarian cancer risk: collaborative analysis of 12 US casecontrol studies. II. Invasive epithelial ovarian cancers in white women. Collaborative Ovarian Cancer Group. Am J Epidemiol, 136, 1184-203. https://doi.org/10.1093/oxfordjournals.aje.a116427
  14. Salazar-Martinez E, Lazcano-Ponce EC, Gonzalez Lira-Lira G, et al (1999). Reproductive factors of ovarian and endometrial cancer risk in a high fertility population in Mexico. Cancer Res, 59, 3658-62.
  15. Risch HA (1998). Hormonal etiology of epithelial ovarian cancer, with a hypothesis concerning the role of androgens and progesterone. J Natl Cancer Inst, 90, 1774-86. https://doi.org/10.1093/jnci/90.23.1774
  16. Rosenblatt KA, Thomas DB (1993). Lactation and the risk of epithelial ovarian cancer. The WHO Collaborative Study of Neoplasia and Steroid Contraceptives. Int J Epidemiol, 22, 192-7. https://doi.org/10.1093/ije/22.2.192
  17. Rossing MA, Tang MT, Flagg EW, Weiss LK, Wicklund KG (2004). A case-control study of ovarian cancer in relation to infertility and the use of ovulation-inducing drugs. Am J Epidemiol, 160, 1070-8. https://doi.org/10.1093/aje/kwh315
  18. Schwarz EB, Ray RM, Stuebe AM, et al (2009). Duration of lactation and risk factors for maternal cardiovascular disease. Obstet Gynecol, 113, 974-82. https://doi.org/10.1097/01.AOG.0000346884.67796.ca
  19. Section on B (2012). Breastfeeding and the use of human milk. Pediatrics, 129, 827-41. https://doi.org/10.1542/peds.2011-3552
  20. Short RV, Lewis PR, Renfree MB, Shaw G (1991). Contraceptive effects of extended lactational amenorrhoea: beyond the Bellagio Consensus. Lancet, 337, 715-7. https://doi.org/10.1016/0140-6736(91)90288-Z
  21. Siskind V, Green A, Bain C, Purdie D (1997). Breastfeeding, menopause, and epithelial ovarian cancer. Epidemiology, 8, 188-91. https://doi.org/10.1097/00001648-199703000-00011
  22. Stadel BV (1975). Letter: The etiology and prevention of ovarian cancer. Am J Obstet Gynecol, 123, 772-4. https://doi.org/10.1016/0002-9378(75)90509-8
  23. Stang A (2010). Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 25, 603-5. https://doi.org/10.1007/s10654-010-9491-z
  24. Permuth-Wey J, Chen YA, Tsai YY, et al (2011). Inherited variants in mitochondrial biogenesis genes may influence epithelial ovarian cancer risk. Cancer Epidemiol Biomarkers Prev, 20, 1131-45. https://doi.org/10.1158/1055-9965.EPI-10-1224
  25. Moorman PG, Palmieri RT, Akushevich L, Berchuck A, Schildkraut JM (2009). Ovarian cancer risk factors in African-American and white women. Am J Epidemiol, 170, 598-606. https://doi.org/10.1093/aje/kwp176
  26. Mori M, Harabuchi I, Miyake H, et al (1988). Reproductive, genetic, and dietary risk factors for ovarian cancer. Am J Epidemiol, 128, 771-7. https://doi.org/10.1093/oxfordjournals.aje.a115030
  27. Ness RB, Grisso JA, Cottreau C, et al (2000). Factors related to inflammation of the ovarian epithelium and risk of ovarian cancer. Epidemiology, 11, 111-7. https://doi.org/10.1097/00001648-200003000-00006
  28. Pieta B, Chmaj-Wierzchowska K, Opala T (2012). Past obstetric history and risk of ovarian cancer. Ann Agric Environ Med, 19, 385-8.
  29. Purdie D, Green A, Bain C, et al (1995). Reproductive and other factors and risk of epithelial ovarian cancer: an Australian case-control study. Survey of Women's Health Study Group. Int J Cancer, 62, 678-84. https://doi.org/10.1002/ijc.2910620606
  30. Riman T, Dickman PW, Nilsson S, et al (2002). Risk factors for invasive epithelial ovarian cancer: results from a Swedish case-control study. Am J Epidemiol, 156, 363-73. https://doi.org/10.1093/aje/kwf048
  31. Riman T, Nilsson S, Persson IR (2004). Review of epidemiological evidence for reproductive and hormonal factors in relation to the risk of epithelial ovarian malignancies. Acta Obstet Gynecol Scand, 83, 783-95. https://doi.org/10.1080/j.0001-6349.2004.00550.x
  32. Risch HA, Weiss NS, Lyon JL, Daling JR, Liff JM (1983). Events of reproductive life and the incidence of epithelial ovarian cancer. Am J Epidemiol, 117, 128-39. https://doi.org/10.1093/oxfordjournals.aje.a113523
  33. Risch HA, Marrett LD, Howe GR (1994). Parity, contraception, infertility, and the risk of epithelial ovarian cancer. Am J Epidemiol, 140, 585-97. https://doi.org/10.1093/oxfordjournals.aje.a117296
  34. Li W, Qiu Y (2007). Relation of supplementary feeding to resumptions of menstruation and ovulation in lactating postpartum women. Chin Med J, 120, 868-70.
  35. Jordan SJ, Cushing-Haugen KL, Wicklund KG, Doherty JA, Rossing MA (2012). Breast-feeding and risk of epithelial ovarian cancer. Cancer Causes Control, 23, 919-27. https://doi.org/10.1007/s10552-012-9963-4
  36. Kurta ML, Moysich KB, Weissfeld JL, et al (2012). Use of fertility drugs and risk of ovarian cancer: results from a U.S.-based case-control study. Cancer Epidemiol Biomarkers Prev, 21, 1282-92. https://doi.org/10.1158/1055-9965.EPI-12-0426
  37. Le DC, Kubo T, Fujino Y, et al (2012). Reproductive factors in relation to ovarian cancer: a case-control study in Northern Vietnam. Contraception, 86, 494-9. https://doi.org/10.1016/j.contraception.2012.02.019
  38. Luan NN, Wu QJ, Gong TT, et al (2013). Breastfeeding and ovarian cancer risk: a meta-analysis of epidemiologic studies. Am J Clin Nutr, 98, 1020-31. https://doi.org/10.3945/ajcn.113.062794
  39. McLaughlin JR, Risch HA, Lubinski J, et al (2007). Reproductive risk factors for ovarian cancer in carriers of BRCA1 or BRCA2 mutations: a case-control study. Lancet Oncol, 8, 26-34. https://doi.org/10.1016/S1470-2045(06)70983-4
  40. McNeilly AS (2001). Lactational control of reproduction. Reprod Fertil Dev, 13, 583-90. https://doi.org/10.1071/RD01056
  41. Mills PK, Riordan DG, Cress RD (2004). Epithelial ovarian cancer risk by invasiveness and cell type in the Central Valley of California. Gynecol Oncol, 95, 215-25. https://doi.org/10.1016/j.ygyno.2004.07.012
  42. Mink PJ, Folsom AR, Sellers TA, Kushi LH (1996). Physical activity, waist-to-hip ratio, and other risk factors for ovarian cancer: a follow-up study of older women. Epidemiology, 7, 38-45. https://doi.org/10.1097/00001648-199601000-00008
  43. Modugno F, Ness RB, Wheeler JE (2001). Reproductive risk factors for epithelial ovarian cancer according to histologic type and invasiveness. Ann Epidemiol, 11, 568-74. https://doi.org/10.1016/S1047-2797(01)00213-7
  44. Huusom LD, Frederiksen K, Hogdall EVS, et al (2006). Association of reproductive factors, oral contraceptive use and selected lifestyle factors with the risk of ovarian borderline tumors: A Danish case-control study. Cancer Causes & Control, 17, 821-9. https://doi.org/10.1007/s10552-006-0022-x
  45. Harlow BL, Weiss NS, Roth GJ, Chu J, Daling JR (1988). Casecontrol study of borderline ovarian tumors: reproductive history and exposure to exogenous female hormones. Cancer Res, 48, 5849-52.
  46. Hartge P, Schiffman MH, Hoover R, et al (1989). A case-control study of epithelial ovarian cancer. Am J Obstet Gynecol, 161, 10-6. https://doi.org/10.1016/0002-9378(89)90221-4
  47. Hirose K, Tajima K, Hamajima N, et al (1999). Comparative casereferent study of risk factors among hormone-related female cancers in Japan. Jpn J Cancer Res, 90, 255-61. https://doi.org/10.1111/j.1349-7006.1999.tb00741.x
  48. Ip S, Chung M, Raman G, Trikalinos TA, Lau J (2009). A summary of the Agency for Healthcare Research and Quality's evidence report on breastfeeding in developed countries. Breastfeed Med, 4, 17-30. https://doi.org/10.1089/bfm.2008.0133
  49. Jacob S, Spencer NA, Bullivant SB, et al (2004). Effects of breastfeeding chemosignals on the human menstrual cycle. Hum Reprod, 19, 422-9. https://doi.org/10.1093/humrep/deh057
  50. Jemal A, Bray F, Center MM, et al (2011). Global cancer statistics. CA Cancer J Clin, 61, 69-90. https://doi.org/10.3322/caac.20107
  51. Jordan SJ, Green AC, Whiteman DC, Webb PM (2007). Risk factors for benign serous and mucinous epithelial ovarian tumors. Obstet Gynecol, 109, 647-54. https://doi.org/10.1097/01.AOG.0000254159.75977.fa
  52. Jordan SJ, Green AC, Whiteman DC, Webb PM (2007). Risk factors for benign, borderline and invasive mucinous ovarian tumors: epidemiological evidence of a neoplastic continuum? Gynecol Oncol, 107, 223-30. https://doi.org/10.1016/j.ygyno.2007.06.006
  53. Jordan SJ, Siskind V, Green AC, Whiteman DC, Webb PM (2010). Breastfeeding and risk of epithelial ovarian cancer. Cancer Causes Control, 21, 109-16. https://doi.org/10.1007/s10552-009-9440-x
  54. do Carmo Franca-Botelho A, Ferreira MC, Franca JL, Franca EL, Honorio-Franca AC (2012). Breastfeeding and its relationship with reduction of breast cancer: a review. Asian Pac J Cancer Prev, 13, 5327-32. https://doi.org/10.7314/APJCP.2012.13.11.5327
  55. Cramer DW, Xu H (1995). Epidemiologic evidence for uterine growth factors in the pathogenesis of ovarian cancer. Ann Epidemiol, 5, 310-4. https://doi.org/10.1016/1047-2797(94)00098-E
  56. CSHS (1987). The reduction in risk of ovarian cancer associated with oral-contraceptive use. N Engl J Med, 316, 650-5. https://doi.org/10.1056/NEJM198703123161102
  57. Danforth KN, Tworoger SS, Hecht JL, et al (2007). Breastfeeding and risk of ovarian cancer in two prospective cohorts. Cancer Causes Control, 18, 517-23. https://doi.org/10.1007/s10552-007-0130-2
  58. Dong JY, Zhang YH, Qin LQ (2011). Erectile dysfunction and risk of cardiovascular disease: meta-analysis of prospective cohort studies. J Am Coll Cardiol, 58, 1378-85. https://doi.org/10.1016/j.jacc.2011.06.024
  59. Fathalla MF (1971). Incessant ovulation--a factor in ovarian neoplasia? Lancet, 2, 163.
  60. Ferlay J SH, Bray F, Forman D, Mathers C and Parkin DM. GLOBOCAN 2008 v2.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 10 [Internet]. Lyon, France: International Agency for Research on Cancer; 2010. Available from: http://globocan.iarc.fr.
  61. Greggi S, Parazzini F, Paratore MP, et al (2000). Risk factors for ovarian cancer in central Italy. Gynecol Oncol, 79, 50-4. https://doi.org/10.1006/gyno.2000.5909
  62. Gronwald J, Byrski T, Huzarski T, et al (2006). Influence of selected lifestyle factors on breast and ovarian cancer risk in BRCA1 mutation carriers from Poland. Breast Cancer Res Treat, 95, 105-9. https://doi.org/10.1007/s10549-005-9051-5
  63. Gwinn ML, Lee NC, Rhodes PH, Layde PM, Rubin GL (1990). Pregnancy, breast-feeding, and oral-contraceptives and the risk of epithelial ovarian-cancer. J Clin Epidemiol, 43, 559-68. https://doi.org/10.1016/0895-4356(90)90160-Q
  64. Chen Y, Wu PC, Lang JH, et al (1992). Risk factors for epithelial ovarian cancer in Beijing, China. Int J Epidemiol, 21, 23-9. https://doi.org/10.1093/ije/21.1.23
  65. Bernier MO, Plu-Bureau G, Bossard N, Ayzac L, Thalabard JC (2000). Breastfeeding and risk of breast cancer: a metaanalysis of published studies. Hum Reprod Update, 6, 374-86. https://doi.org/10.1093/humupd/6.4.374
  66. Booth M, Beral V, Smith P (1989). Risk factors for ovarian cancer: a case-control study. Br J Cancer, 60, 592-8. https://doi.org/10.1038/bjc.1989.320
  67. CDC Breastfeeding Report Card-United States, 2012, CDC National Immunization Survey. Available from: http://www.cdc.gov/breastfeeding/pdf/2012BreastfeedingReportCard.pdf.
  68. Chiaffarino F, Pelucchi C, Negri E, et al (2005). Breastfeeding and the risk of epithelial ovarian cancer in an Italian population. Gynecol Oncol, 98, 304-8. https://doi.org/10.1016/j.ygyno.2005.05.006
  69. Collaborative Group on Hormonal Factors in Breast C (2002). Breast cancer and breastfeeding: collaborative reanalysis of individual data from 47 epidemiological studies in 30 countries, including 50302 women with breast cancer and 96973 women without the disease. Lancet, 360, 187-95. https://doi.org/10.1016/S0140-6736(02)09454-0
  70. Adami HO, Hsieh CC, Lambe M, et al (1994). Parity, age at first childbirth, and risk of ovarian cancer. Lancet, 344, 1250-4. https://doi.org/10.1016/S0140-6736(94)90749-8
  71. Antoniou AC, Rookus M, Andrieu N, et al (2009). Reproductive and hormonal factors, and ovarian cancer risk for BRCA1 and BRCA2 mutation carriers: results from the International BRCA1/2 Carrier Cohort Study. Cancer Epidemiol Biomarkers Prev, 18, 601-10. https://doi.org/10.1158/1055-9965.EPI-08-0546
  72. Berlin JA, Longnecker MP, Greenland S (1993). Meta-analysis of epidemiologic dose-response data. Epidemiology, 4, 218-28. https://doi.org/10.1097/00001648-199305000-00005
  73. Cramer DW, Hutchison GB, Welch WR, Scully RE, Ryan KJ (1983). Determinants of ovarian cancer risk. I. Reproductive experiences and family history. J Natl Cancer Inst, 71, 711-6.

Cited by

  1. Ovarian Cancer in Iranian Women, a Trend Analysis of Mortality and Incidence vol.15, pp.24, 2015, https://doi.org/10.7314/APJCP.2014.15.24.10787
  2. Nutrition and physical activity of infants and breastfeeding women vol.164, pp.9, 2016, https://doi.org/10.1007/s00112-016-0147-2
  3. Nutrition and physical activity of infants and breastfeeding women vol.164, pp.S5, 2016, https://doi.org/10.1007/s00112-016-0173-0
  4. Cancer incidence in Ireland—the possible role of diet, nutrition and lifestyle vol.25, pp.2, 2017, https://doi.org/10.1007/s10389-016-0769-9
  5. Adherence of Primary Care Physicians to Evidence-Based Recommendations to Reduce Ovarian Cancer Mortality vol.25, pp.3, 2016, https://doi.org/10.1089/jwh.2015.5735
  6. Association between breastfeeding and risk of endometrial cancer vol.27, pp.2, 2018, https://doi.org/10.1097/CEJ.0000000000000186
  7. Preoperative assessment of ovarian tumors using a modified multivariate index assay vol.11, pp.1, 2018, https://doi.org/10.1186/s13048-018-0419-7